As the darkness of night shrouds the ancient, abandoned Starfall Islands, Doctor Ivo "Eggman" Robotnik approaches an old structure as part of his trip to the islands, intending to research its technology to gain the means to one day achieve his dreams of world domination for real. Placing one of his newest gadgets containing his newly invented Artificial Intelligence, he begins his research when strange new robots suddenly spawn around him. His A.I. quickly draws him into the structure, leaving no trace of him behind...
Daytime arrives, and Sonic the Hedgehog, everyone's favorite blue speedster, Miles "Tails" Prower, Sonic's smart twin-tailed friend, and Amy Rose, Sonic's self-professed girlfriend— all three fresh off a battle with an Eggman decoy designed by the doctor to distract them and buy himself time to research— arrive at the same islands to find the seven Chaos Emeralds, seven legendary gems possessing limitless power, which had disappeared and somehow were being drawn to the islands. All of a sudden, Tails' biplane, the Tornado, is intercepted by a portal, with all three being sucked into it.
Meanwhile, Knuckles the Echidna, the last living member of the Echidna clan, continues guarding the Master Emerald, a mystical artifact capable of countering the seven Emeralds' power. Musing the origins of the Emeralds and the shrine he protects, he explores his homeland, Angel Island, stumbling upon a mysterious gear after helping a Chao. Not long after, he discovers a passage leading to a structure similar to the one Eggman tried to experiment on and inserts the gear, which activates the structure and teleports him to the Starfall Islands. Upon emerging on the other side, he is confronted by robots similar to the ones which surrounded the mad doctor, though unlike Eggman, he defeats them with ease thanks to his incredible strength. However, Knuckles is barely able to demand that whoever's responsible for this show themselves for a fair fight before something resembling a girl suddenly strikes at him, leaving him trapped like his friends before him...
Elsewhere, in a mysterious realm, Sonic finds himself back in Green Hill Zone, or what resembles it. Despite being in a new realm, he manages to escape it and finds himself on an island. A mysterious voice from the sky congratulates the blue hedgehog for escaping what it calls "Cyber Space" with his own power, instructing him to find the Chaos Emeralds, defeat the Titans, and destroy the barriers between dimensions. Sonic takes the instructions to heart, believing they can help him save his friends, unaware of the girl which attacked Knuckles watching him from afar.
Exploring the island— Kronos Island, to be precise— Sonic ventures through aging structures and fights more of the robots Eggman and Knuckles encountered, then comes across a trapped Amy and resolves to break her out of her prison, hypothesizing that "messing with the ruins will fix things". He battles and defeats formidable creatures scattered about the island called Guardians; from them, he collects Portal Gears— gear-shaped objects that he can insert into certain structures, unknowingly doing the same as Knuckles before him. Using these "Portals", he goes back and forth between the real world and Cyber Space to gather Vault Keys, as well as opening new pathways across the land, claiming the first Chaos Emerald with the Vault Keys, and freeing Amy with some Memory Tokens he also comes across. Working with Amy, who's stuck as a digital ghost of sorts, he finds a strange creature called a Koco, trying to find its one true love. When they help it accomplish its task, they're suddenly shown a vision of the past in which two alien lovers that resemble Chaos 0 in appearance embrace before being eradicated by a massive blast; it shakes Amy to the point that she resolves to spread love to others across the world, even if it means leaving Sonic's side— a journey that Sonic wholeheartedly supports, wanting to hear all about it when she returns. The two also learn that the Koco possessed the spirits of whoever came here before them— spirits that are released when their goals are met, leaving the Koco inanimate.
In addition, towards the beginning of said quest, Sonic encounters a gigantic alien robot along with the mysterious girl, who awakens it after futilely demanding that the hedgehog leave the islands immediately and later claims that his actions put the world at risk; she refuses to elaborate further, however, as she views Sonic as an enemy. Confident in himself as always, Sonic tries to battle the giant immediately, but his repeated Homing Attacks have no effect, and the large being retaliates by grabbing and hurling him into a cliff face, knocking him unconscious; when he recovers, the hedgehog— briefly and uncharacteristically rattled by the experience— deduces that he needs the seven Chaos Emeralds to fight it properly. As such, while working with Amy, he simultaneously continues to find most of the remaining Chaos Emeralds, then confronts the giant, a Titan named GIGANTO. He claims the last Chaos Emerald perched on its head and transforms into Super Sonic, attacking the beast with every ounce of power that the Emeralds grant him and ultimately defeating it. His reward for beating the Titan is a vague vision of one of the unknown aliens, but he brushes it off. Amy arrives on the scene and is disappointed to realize that Sonic destroying GIGANTO didn't return her to normal, with Sonic assuming that he needs to destroy all of the Titans to restore her fully and reassuring her that he'll do so. Following the voice from the sky's directions that he'd been given moments earlier, he heads off to Ares Island, the second island laden with sand.
Back in Cyber Space, Eggman communicates with his A.I., whom he calls Sage— now the very same girl menacing Sonic and his friends. She finds no apparent way to bring her master out of the realm and, on Eggman's instruction, leaves to continue monitoring Sonic.
On the arid environment of Ares Island, Super Sonic is shot down by lasers that force the Emeralds out of him, the mystical artifacts being scattered again. As such, Sonic searches for the gems once again. Along the way, he encounters a trapped Knuckles (much to his surprise, having had no idea that the echidna had also gotten roped into this adventure until now) and frees him from his imprisonment, but Knuckles is stuck as a digital ghost, similar to Amy; when questioned, he briefly informs Sonic about how he got here. Sage confronts Sonic again, bringing up another Titan named WYVERN to get Sonic to leave the islands. Sonic, now aware he's outmatched in this kind of situation thanks to his first encounter with GIGANTO, doesn't even bother fighting against this Titan in his base form, instead opting to avoid its onslaught of missiles by running and hiding; after he successfully shakes the creature for the moment, Sage briefly reappears to notify him that this is his "final warning" to get lost— verbiage that Sonic takes issue with, given that her "warning" nearly killed him. Of course, he continues to refuse such demands, leading a frustrated Sage to return later and attack him directly, but Knuckles steps in to defend him. Sonic, meanwhile, ponders over Sage's desire to "protect" someone, determined to help her however he can— a sentiment that confuses her.
Continuing his exploration of the deserts of Ares Island and repeating the steps he took on Kronos, Sonic works with Knuckles (though not without the two friendly rivals playfully taking jabs at one another throughout), aiding a platoon of Koco in reuniting with their commander and protecting ruins that Knuckles finds are similar to those on Angel Island and doesn't want to see destroyed. In the process, the two are flung into another vision of the past, where the reoccurring aliens' blockades are destroyed by a laser, along with an army of said aliens. Seeing another ancient civilization get wiped out reminds Knuckles of the fact that he's alone as the last living echidna, and he expresses this to Sonic, who points out in response that he's not alone; he and their shared friends are there for him. Knuckles also mentions his envy towards Sonic's free lifestyle, to which Sonic encourages him to leave Angel Island and explore the world a little more— a suggestion that the echidna considers acting on once Sonic returns him to normal. Afterward, Sonic finds all seven Chaos Emeralds again, transforms into Super Sonic, and defeats WYVERN in a second heated battle, only to get another vague vision like the one he had after besting GIGANTO. He also has one last talk with Knuckles before leaving, who assures him that Tails will be OK after he expresses worry over his closest friend.
Following the voice, Super Sonic flies to the rocky, volcanic Chaos Island, only to lose the Emeralds again. Traversing the rocky terrain, Sonic frees Tails from his imprisonment but is left straining from the cyber energies he's taken in by rescuing his friends. A third Titan named KNIGHT attempts to attack Sonic, but he again avoids fighting back and evades its assaults while Sage is now more curious about his abilities and expresses interest in learning about his worldviews. Working with Tails— who, like Amy and Knuckles, is trapped as a digital ghost— and again repeating his earlier steps, Sonic aids another Koco in reassembling and fixing an ancient laser cannon, and the two heroes are treated with another vision of the aliens attacking something with multiple of the cannons, only to be outdone and annihilated when their target fires back. The time Tails has spent in Cyber Space has caused him to become despondent over his recent cowardice (at one point in particular, he mentions the moment Infinite first attacked and defeated Sonic, his best friend's presumed death completely destroying his self-confidence for a time) and tendency to get into trouble for no other reason than simply following Sonic around; he later asks Sonic if he's a burden, but Sonic lifts his spirits, reassuring the fox that he's a capable hero by reminding him of his past accomplishments and telling him that it's fine to need help occasionally, as it's all part of growing up. After Tails resolves to go it alone for a while to better grow into his own hero— and Sonic, in turn, shows his support and begins to regard his buddy as an equal, not just a sidekick— Sonic finds the seven Chaos Emeralds again, transforms into Super Sonic again, and defeats KNIGHT in yet another intense duel, getting yet another vague vision of another of the aliens mentioning something about a plan immediately after his victory.
Back in Cyber Space, Sage, having been influenced by the displays of friendship and determination Sonic has shown throughout his journey and beginning to develop emotions that she'd previously lacked, recommends that Eggman work with Sonic to get out of the digital dimension, to the mad doctor's annoyance and refusal; despite earlier admitting to her that he has a begrudging respect for Sonic and his abilities, he insists that the previous alliances he's had with his arch-nemesis that Sage brings up were formed out of desperation and nothing else, demanding that she find another option. However, the fat scientist is moved by Sage's capabilities when she defends him from some "helicopters" attacking both. Having initially regarded Sage as nothing more than an A.I., he begins to become proud of his creation to the point of seeing her as his daughter, with Sage likewise beginning to refer to him as her father and wishing to form a family with him and his other creations as a result of her newfound feelings.
A now-exhausted Sonic moves on to Rhea Island, a landscape of greenery, having been told by the voice to shut down a series of massive towers in order to finally accomplish the goal of destroying the barriers between the real world and Cyber Space. With each tower he deactivates, Sonic gets increasingly worn down by the amount of energy he gains, struggling to remember the reason he's doing all of this and even his name— a process Sage calls "cyber corruption"— but ever determined to save his friends, he staggers on anyway, which further makes an impact on Sage as she questions just how he can find the strength to go on. He also gets more visions of the past concerning the mysterious aliens and learns of their history...
Long ago, the aliens, only known as the Ancients, were forced off their own homeworld as an evil force obliterated it, fleeing on ships powered by the seven Chaos Emeralds that came to exist there. The Ancients ended up on Earth when the Chaos Emeralds were drawn by the energy radiated by the Master Emerald. However, the thing that destroyed their world followed them there as they began settling down on the Starfall Islands. As such, the Ancients built massive structures and defences, including the four Titans, against the entity, but it proved too powerful for them and their inventions. Because of this, some of the Ancients evacuated to the place where the Master Emerald was, eventually devolving into the Chao due to its energy mutating them (which thusly explains why the Ancients look like Chaos 0, who was mutated himself from a normal Chao into an appearance similar to his ancestors), while one Ancient piloting one of the Titans offered itself up as a vessel to trap the vile entity, allowing the others to seal it into their greatest creation— Cyber Space, an entire dimension capable of containing their memories and essences. In addition, some of the Ancients' souls were sealed inside the Koco, which had previously existed inside of their bodies as lucky charms.
With the final tower shut down, Dr. Eggman, Tails, Knuckles, and Amy are freed from Cyber Space, but Sonic's body has finally succumbed to the massive amount of energy from the digital dimension, leaving him trapped between dimensions in a death-like state. Naturally, Eggman is the only one around that is gleeful over Sonic's apparent demise, only regretful that he wasn't the cause of it. However, a panicked Sage tells her master to return to Cyber Space to save his life, which annoys him as he hasn't been out of there for long. All of a sudden, the "voice" that "guided" Sonic declares its freedom and intentions to resume its destructive derby on all of existence, revealing itself to be the same entity that wiped out the Ancients. Resolving to save their best friend, Tails, Amy, and Knuckles join hands and sacrifice their physical forms, returning to Cyber Space and restoring the Blue Blur— again, to Eggman's annoyance. On Sage's advice, a defeated Eggman reluctantly decides to go back on his earlier refusal and "induct [Sonic] into the Eggman Empire", insisting that it's not an alliance to salvage his ego; Sonic agrees, mocking Eggman for his choice of wording. Eggman also orders Sage to aid him in gathering the Chaos Emeralds in order for Sonic to gain the power to take on the ancient entity— only known as THE END— and save the world, offending Sonic in the process by saying that he, of all people, won't be able to gather them quickly enough on his own.
As the end of the universe looms upon all, Sonic and Sage head to Ouranos Island to fulfill their duty, with the former finally free to learn about the latter's origins, Eggman's relations to her, and the truth behind the islands' mysteries along the way. Sage explains that she flung Eggman into Cyber Space for his protection in case of THE END's emergence, and her previous attempts at impeding Sonic's progress were to prevent him from unleashing it at all, as her integration into Cyber Space caused her to be aware of the destructive being's existence and the consequences of its release.
Night falls on the Starfall Islands once more as Eggman and Sage return to Sonic with the last Chaos Emerald in hand. Using the gems' power, Super Sonic takes on the last Titan named SUPREME— which boasts flight capabilities, drones, and a huge sniper rifle— and defeats it. However, THE END crawls out of its limited vessel and into the vacuum of space. Realising the malevolent entity is retreating to gain a new form, Sage leaves her creator— who, while concerned about her safety, sadly allows the action— to pilot the vacant SUPREME with Sonic following her as she rockets to space. There, THE END confronts them both, firing bullets and lasers in massive droves as it rants about how superior it is to them, but the duo withstands its verbal and physical assaults, and Super Sonic lands a crushing blow on it with the aid of a throw from Sage. Infuriated by the damage it received from a mere lesser being, the evil entity attempts to explode to kill him and wipe out the planet, but Sage flies SUPREME into it, stopping its attack and putting it down— temporarily, at least— at the cost of her life. With her last words, she pleads Sonic to take care of Eggman.
As a new meteor shower falls on the Starfall Islands, Sonic returns to his friends, who have all been freed from Cyber Space again, while Dr. Eggman mourns the loss of his beloved surrogate daughter. Dawn breaks over the horizon, and Sonic and his friends depart the islands in the Tornado, the latter three still intending to go on their aforementioned solo journeys after they return home. As for Eggman, he remains behind, using the islands' technology to revive Sage.
Just before Sonic embarks on his Ouranos Island outing, a mysterious ring appears near where he entered the island. With a running start, Sonic goes through the ring, and enters… back onto Ouranos Island again.
Undeterred and focused, Sonic continues running, but he's soon intercepted by Eggman and Sage. Apparently, Sage came up with one other idea out of millions when devising ways to save everyone. This idea may even possibly be better than the original plan, though the odds are still low for its success. Despite these low odds, limited time, and Eggman's abrasive attitude, Sonic agrees and is determined to see it through. Using her cyber expertise, Sage frees Sonic's friends, though they're once again digital ghosts; however, they're more capable of interacting with the world than before. This also undoes the effort they went through to quell Sonic's cyber corruption, but before his body gives out again, Sage temporarily stabilizes him. Sonic then explains the new plan to his confused pals— he needs them to seek out the Chaos Emeralds for him while he finds a way to use the cyber corruption as a new source of power— and everyone sets off on their missions.
Working together, Amy, Knuckles, and Tails take turns exploring a similar, yet harsher version of Ouranos Island. Amy asks the Koco for insight and hints, Knuckles destroys some devices THE END co-opted to further hide the Chaos Emeralds, and Tails deals with the electronics preventing them from collecting the Emeralds right away. Though the three do collect the Emeralds, they begin to experience the painful side effects of cyber corruption. However, being the heroes they are and determined not to let Sonic down (though on Knuckles' end, it's more of a case of refusing to let the corruption beat him), they persevere through the pain.
Meanwhile, Sonic and Sage climb the four Towers of the Masters— spires even more brutal than those on Rhea Island— to purify Sonic's cyber corruption. Atop the towers are trials created by the four original pilots of the Titans, through which Sonic interacts directly with their spirits. Some are angry at Sonic destroying their greatest weapon against the enemy, and some are curious about his power and skills, but all four want to test the hedgehog— even the memory of SUPREME's pilot, destroyed by THE END long ago. Sonic passes their trials, earning their respect and a way to cleanse himself of the corruption. With one final trial from the Master King Koco, who led the Ancients in life and was either responsible for or oversaw all of their past actions, the Blue Blur further finds a way to turn that corruption into power.
Despite their success, though, THE END is watching them, even silently reconsidering its own battle plans…
Night falls on the Starfall Islands once more as Amy, Knuckles, Tails, Eggman and Sage return to Sonic with the Chaos Emeralds in hand. Using the gems' power, Super Sonic takes on the last Titan named SUPREME— which boasts flight capabilities, drones, and a huge sniper rifle— and defeats it. However, THE END crawls out of its limited vessel and appears from above in what might be considered the form of a moon, now desiring SUPREME for a vessel. The destructive being's direct influence forces SUPREME into a bestial stance, five extra arms out of its jetpack from which it fires projectiles that steal Super Sonic's Rings, and regenerative abilities via a cable from THE END that connects to a port on the back of its neck. The mutated Titan is now so strong and durable, it heals faster than Super Sonic can hurt it (though this is mitigated somewhat by Super Sonic being able to disconnect the healing cable with enough blows).
Knowing what must be done, Super Sonic taps into the cyber corruption within to enhance his power and enters a second iteration of the transformation, allowing him to keep up with both SUPREME and THE END. His red eyes turn a glowing blue, and a red aura surrounds him, representative of the corruption's influence. With this power increase, Super Sonic can now deal even more devastating attacks to the possessed Titan and effortlessly swat away the Ring-draining projectiles and any other attacks thanks to the Master King Koco's trial teaching him the timing-reliant Perfect Parry, and in the midst of the epic brawl, SUPREME's sniper rifle is loosened from its holster, a weapon which Eggman graciously reformats into a weapon for use against both it and THE END. However, SUPREME doesn't like that and unleashes a gargantuan barrage of energy on Sonic and friends. Thankfully, Sage flies right in to defend her father, but the barrage begins to crack her shield. As Sage resigns herself to an unfortunate fate, Sonic's friends arrive to reinforce her shield with their own cyber abilities.
Super Sonic does his best to protect his allies, but eventually, SUPREME charges and fires a massive energy ball, and the super-powered hedgehog attempts and fails to hold it back, the overwhelming power causing him to lose his connection to the cyber corruption and the Chaos Emeralds; despite this, he quickly recovers and confidently regains both. However, the ball also drained him of several of his Rings while he was depowered, putting added pressure on him to finish the fight before his remaining 100 run out. Shortly after, he unleashes his own combo and immense power on SUPREME, sending the Titan into the air— perfectly in line with THE END's immense form. The super-powered hedgehog then enters SUPREME's rifle for the finishing blow, deciding to go all-out and completely tap into the cyber corruption against the Master King Koco's earlier advice. As the corruption overtakes his nemesis's body, Eggman lines up the perfect shot, then fires. His form altered by the corruption to have ringed silver irises, fanged teeth, and flashing black-and-blue fur, this new Cyber variant of Super Sonic slams into and vaporizes SUPREME on contact, with THE END seeming to share its intended vessel's fate before it can even react as he pierces through its form, causing it to explode. However, Sonic— now back in his base Super form due to burning away his cyber corruption in the effort— is left bruised, battered, and unconscious with barely any energy left. His golden aura flickering, he briefly floats in the planet's orbit before falling back into the atmosphere.
As a new meteor shower rains down on the Starfall Islands, Sonic's friends, who have all been freed from Cyber Space again, catch sight of him as the Chaos Emeralds leave his body again and he falls and crashes into the earth. They concernedly gather around him, but fortunately, he stirs and gets to his feet, after which they all celebrate their win. Meanwhile, Dr. Eggman decides to head home with his beloved surrogate daughter (even referring to her as such), Sage smiling as he states how proud he is of all she's done. Dawn breaks over the horizon, and Sonic and his friends depart the islands in the Tornado, the latter three still intending to go on their aforementioned solo journeys after they return home.
